Arch. Environ. Contam. Toxicol. 52, 572–579 (2007) DOI: 10.1007/s00244-006-0200-6
Trophic Transfer of Polychlorinated Biphenyls in Great Blue Heron (Ardea herodias) at Crab Orchard National Wildlife Refuge, Illinois, United States C. L. Straub,1,2 J. D. Maul,1 R. S. Halbrook,2 B. Spears,3 M. J. Lydy1 1 2 3
Fisheries and Illinois Aquaculture Center and Department of Zoology, Southern Illinois University, Carbondale, Illinois 62901, USA Cooperative Wildlife Research Laboratory and Department of Zoology, Southern Illinois University, Carbondale, Illinois 62901, USA Upper Columbia Fish and Wildlife Office, United States Fish and Wildlife Service, 11103 East Montgomery Drive, Spokane, Washington 99206, USA
Received: 18 September 2006 /Accepted: 5 November 2006
Abstract. In this study, polychlorinated biphenyl (PCB) concentrations were measured in great blue heron (GBHE) (Ardea herodias) chicks and eggs at Crab Orchard National Wildlife Refuge (CONWR) in southern Illinois. In addition, biomagnification factors (BMFs) from gizzard shad (Dorosoma cepedianum) and their effects on reproductive effort were examined. Total PCBs (SPCBs) in chicks and shad were greater at the east end of Crab Orchard Lake (i.e., near the site of contamination) than the west end, but chick concentrations (4.1 to 10.1 mg/kg lipid weight) were lower than those typically associated with adverse effects. Chick BMFs based on shad from diet samples were greater than those based on shad collected from the lake. Furthermore, the two shad sources had dissimilar dioxin-like congener patterns and SPCBs, suggesting that there was variation in PCB load and composition and that the more contaminated shad were a small proportion of the actual heron chick diet. The number of eggs laid per nest was similar between colonies, suggesting no observable population level effects. Further study may be necessary to evaluate longterm effects on GBHEs at CONWR.
Crab Orchard National Wildlife Refuge (CONWR) in southern Illinois has a history of polychlorinated biphenyl (PCB) contamination, and in 1987, CONWR was placed on the National Priorities List. Currently, sediments at the east end of Crab Orchard Lake (COL) contain measurable PCB concentrations (e.g., 9.6 mg/kg organic carbon [oc]) (Maul et al. 2006). In terms of aquatic species, PCB concentrations in zooplankton (copepods and cladocerans) and macrobenthos (oligochaetes and chironomids) at COL have ranged from 0.02 to 0.3 mg/kg weight wet (ww) and 0.07 to 1.1 mg/kg ww, respectively (Hite and King 1977). Furthermore, 38% of fish fillets from gizzard shad (Dorosoma cepedianum), largemouth bass (Micropterus salmoides), bluegill (Lepomis macrochirus), white crappie (Pomoxis annularus), channel catfish (Ictalurus punctatus), and common carp (Cyprinus carpio) at COL had PCB Correspondence to: M. J. Lydy; email:
[email protected]
concentrations >2.0 mg/kg ww (Kohler et al. 1990), indicating bioaccumulation in fish species. Terrestrial avian species within CONWR have also been impacted. For example, hatching success was decreased in European starlings (Sturnus vulgaris) (McKee 1995), and increased chick mortality, decreased fledgling success, and decreased nest attentiveness in European starlings have been reported (Arenal and Halbrook 1997; Arenal et al. 2004). Impacts of PCBs to higher–trophic level organisms occur because these compounds bioaccumulate by way of trophic transfer, typically beginning with sediment-dwelling invertebrates (Kukkonen and Landrum 1995). Such processes have occurred at CONWR with transfer of PCBs from the aquatic environment to tree swallows (Tachycineta bicolor) by way of emergent aquatic insects (Maul et al. 2006). In the current study, trophic transfer of PCBs from gizzard shad to a piscivorous avian species, great blue heron (GBHE) (Ardea herodias), was examined. This trophic pathway is particularly important because many fish species at CONWR contain increased PCB concentrations, but bioaccumulation and PCB impacts to fish-eating predators has never been examined. Other studies have indicated that GBHEs, and other piscivorous birds, readily bioaccumulate PCBs by way of trophic transfer (Gould et al. 1997, Thomas and Anthony 1999). Increased PCB levels in piscivorous avian species can lead to decreased growth (Gould et al. 1997), delayed egg laying, and longer incubation periods (Murk et al. 1996). Furthermore, PCBs in fish can decrease egg production and the viability of fish eggs and larvae (Barnthouse et al. 2003), thus impacting GBHEs ecologically by decreasing overall food resources. The objectives of this study were to: (1) measure concentrations of PCBs in GBHE chicks, GBHE eggs, and shad at COL; (2) calculate chick biomagnification factors (BMFs) of total PCBs and toxic equivalents of 2,3,7,8-tetrachlorodibenzop-dioxin–like congeners; (3) compare BMFs and PCB congener patterns in shad from diet samples and those collected from COL to gain insight into the route of PCB bioaccumulation in GBHEs and the utility of examining lake-collected prey items for estimating risk; and (4) examine variation in GBHE reproductive effort between colonies of varying distance from the source of contamination.
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Trophic Transfer of Polychlorinated Biphenyls in Great Blue Heron
Materials and Methods Study Sites CONWR is located approximately 8 km west of Marion, IL, in Williamson County (9S, 1E, NW30). The refuge includes COL, which is 14.5 km long and has a surface area of 28.19 km2 (6,965 acres), a mean depth of approximately 3 m, and maximum depth slightly more than 10 m (Hite and King 1977; United States Environmental Protection Agency [USEPA] 2002). Industrial use of this area began in the 1940s, and several industries disposed of waste in landfills and dumps within the refuge (USEPA 2002). PCB-contaminated by-products were buried in a landfill (Area 9 Landfill) near COL and were spilled at a building complex just south of the landfill. Initial remediation at the Area 9 Landfill and building complex commenced in December 1995 and was completed in June 1997. Remediation included excavation of approximately 41,226 m3 PCB-contaminated sediment from an embayment at the east end of the lake, hereafter called ‘‘Area 9 Landfill embayment’’ (USEPA 2000). Two GBHE colonies were monitored during this study, varying in distance along a gradient from the known source of PCB contamination. One colony, located at the east end of COL, 3.1 km from the Area 9 Landfill embayment area of the lake (Fig. 1), had sediment PCB concentrations of 124 € 16 lg/kg dry weight (dw) (Maul et al. 2006). The second colony, located at the west end of COL (Fig. 1), approximately 12.6 km from the Area 9 Landfill embayment, had no known local areas of PCB contaminated sediment, and PCB sediment concentrations were lower than the method detection limit (DL) (i.e., < 0.005 mg/kg dw).
Egg Monitoring and Analysis Monitoring of GBHE colonies began in early February 2004 and 2005, coinciding with the return of heron to COL. Each colony was visited weekly to observe nesting activity, and nests were sampled approximately 3 weeks after the onset of incubation. The number of eggs in observable nests was recorded, and randomly selected eggs were collected from nests within each colony. Nests and eggs were uniquely labeled, and collected eggs were accounted for when estimating the number of eggs per nest. Collected eggs were placed in coolers and transported to the Cooperative Wildlife Research Laboratory (CWRL) at Southern Illinois University, Carbondale, IL. In the laboratory, whole eggs and egg contents were weighed ( € 0.01 g) on a Mettler balance (AE240, Mettler, Ksnacht, Switzerland), and egg contents were placed in acid-washed jars before PCB analysis.
Chick Monitoring and Analysis At approximately 5 weeks posthatch, chicks were collected from nests. The number of chicks per nest was recorded for all observable nests during these sampling events, and the collected chicks were accounted for in chick-per-nest calculations. Chicks were collected from the same nests from which eggs were collected and/or from other successful nests. Additional nests, where the number of chicks could be counted, were also used to estimate reproductive effort. After collection, chicks were placed in a ventilated box and transported to CWRL. In the laboratory, chicks were killed by asphyxiation with carbon dioxide, weighed ( € 0.1 g) on a balance (Sartorius, Gçttingen, Germany), and total length ( € 1.0 mm) was measured with a commercial tape measure. Chicks were necropsied, and the sex of each chick was determined, abdominal and subcutaneous fat (>0.5 g) was collected for PCB analysis, and stomach contents were removed. If the stomach contained an intact identifiable fish, it was collected for PCB analysis.
Fig. 1. Locations of the west end GBHE (A. herodias) colony (WC), east end GBHE colony (EC), and the Area 9 Landfill and building complex and associated embayment (A9) on COL within the CONWR, Williamson County, IL. In addition, freshly regurgitated fish were collected either directly from the nest or from the area below the tree during visits to the colonies, wrapped in aluminum foil, and transported to the CWRL for PCB analysis. All fish collected from the stomach and regurgitate and identifiable as shad are hereafter referred to as ‘‘diet shad.’’
Shad Collection and Analysis Shad were collected from the Area 9 Landfill embayment in mid June 2004 and 2005 by way of boat-mounted electrofishing equipment and are referred to herein as ‘‘lake shad.’’ PCB concentrations in these fish should represent gizzard shad with the highest PCB concentrations. Shad from the west end of the lake were collected
